Structural constraints and dynamics of bacterial cell wall architecture

Frontiers in Microbiology

Volumn 6, Issue MAY, 2015, Pages

  de Pedro, Miguel A ^a,b   Cava, Felipe ^b  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

Cell wall; Chain length; Cross link; HPLC; Muropeptides; Peptidoglycan; Structure

Indexed keywords

GLYCAN; PEPTIDOGLYCAN;

BACTERIAL CELL WALL; BACTERIAL GROWTH; BIODIVERSITY; CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; CROSS LINKING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MICROBIAL MORPHOLOGY; MORPHOGENESIS; NONHUMAN; REVIEW;

BACTERIA (MICROORGANISMS);

EID: 84931270325     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00449     Document Type: Review

References (60)

1. Barnickel, G., Labischinski, H., Bradaczek, H., and Giesbrecht, P. (1979). Conformational energy calculation on the peptide part of murein. Eur. J. Biochem. 95, 157-165. doi: 10.1111/j.1432-1033.1979.tb12950.x.
2. Barnikel, G., Naumann, D., Bradaczek, H., Labischinski, H., and Giesbrecht, P. (1983). "Computer-aided molecular modelling of the three dimensional structure of bacterial peptidoglycan," in The Target of Penicillin: The Murein Sacculus of Bacterial Cell Walls, Architecture and Growth, eds J.-V. H. R. Hakenbeck and H. Labischinski (Berlin: de Gruyter), 61-66.
3. Boniface, A., Parquet, C., Arthur, M., Mengin-Lecreulx, D., and Blanot, D. (2009). The elucidation of the structure of Thermotoga maritima peptidoglycan reveals two novel types of cross-link. J. Biol. Chem. 284, 21856-21862. doi: 10.1074/jbc.M109.034363.
4. Brown, P. J., de Pedro, M. A., Kysela, D. T., Van Der Henst, C., Kim, J., De Bolle, X., et al. (2012). Polar growth in the Alphaproteobacterial order Rhizobiales. Proc. Natl. Acad. Sci. U.S.A. 109, 1697-1701. doi: 10.1073/pnas.1114476109.
5. Bui, N. K., Gray, J., Schwarz, H., Schumann, P., Blanot, D., and Vollmer, W. (2009). The peptidoglycan sacculus of Myxococcus xanthus has unusual structural features and is degraded during glycerol-induced myxospore development. J. Bacteriol. 191, 494-505. doi: 10.1128/JB.00608-08.
6. Cameron, T. A., Anderson-Furgeson, J., Zupan, J. R., Zik, J. J., and Zambryski, P. C. (2014). Peptidoglycan synthesis machinery in Agrobacterium tumefaciens during unipolar growth and cell division. MBio 5, e01219-e01214. doi: 10.1128/mBio.01219-14.
7. Caparros, M., Quintela, J. C., and de Pedro, M. A. (1994). Variability of peptidoglycan surface density in Escherichia coli. FEMS Microbiol. Lett. 121, 71-76. doi: 10.1016/0378-1097(94)90147-3.
8. Cava, F., de Pedro, M. A., Lam, H., Davis, B. M., and Waldor, M. K. (2011). Distinct pathways for modification of the bacterial cell wall by non-canonical D-amino acids. EMBO J. 30, 3442-3453. doi: 10.1038/emboj.2011.246.
9. Churchman, J. W. (1927). The structure of B. anthracis and reversal of the Gram Reaction. J. Exp. Med. 46, 1007-1029. doi: 10.1084/jem.46.6.1007.
10. Costa, K., Bacher, G., Allmaier, G., Dominguez-Bello, M. G., Engstrand, L., Falk, P., et al. (1999). The morphological transition of Helicobacter pylori cells from spiral to coccoid is preceded by a substantial modification of the cell wall. J. Bacteriol. 181, 3710-3715.
11. Gan, L., Chen, S., and Jensen, G. J. (2008). Molecular organization of Gram-negative peptidoglycan. Proc. Natl. Acad. Sci. U.S.A. 105, 18953-18957. doi: 10.1073/pnas.0808035105.
12. Glauner, B. (1988). Separation and quantification of muropeptides with high-performance liquid chromatography. Anal. Biochem. 172, 451-464. doi: 10.1016/0003-2697(88)90468-X.
13. Glauner, B., and Höltje, J. V. (1990). Growth pattern of the murein sacculus of Escherichia coli. J. Biol. Chem. 265, 18988-18996.
14. Glauner, B., Holtje, J. V., and Schwarz, U. (1988). The composition of the murein of Escherichia coli. J. Biol. Chem. 263, 10088-10095.
15. Gumbart, J. C., Beeby, M., Jensen, G. J., and Roux, B. (2014). Escherichia coli peptidoglycan structure and mechanics as predicted by atomic-scale simulations. PLoS Comput. Biol. 10:e1003475. doi: 10.1371/journal.pcbi.1003475.
16. Gupta, R., Lavollay, M., Mainardi, J. L., Arthur, M., Bishai, W. R., and Lamichhane, G. (2010). The Mycobacterium tuberculosis protein LdtMt2 is a nonclassical transpeptidase required for virulence and resistance to amoxicillin. Nat. Med. 16, 466-469. doi: 10.1038/nm.2120.
17. Harz, H., Burgdorf, K., and Holtje, J. V. (1990). Isolation and separation of the glycan strands from murein of Escherichia coli by reversed-phase high-performance liquid chromatography. Anal. Biochem. 190, 120-128. doi: 10.1016/0003-2697(90)90144-X.
18. Hobot, J. A., Carlemalm, E., Villiger, W., and Kellenberger, E. (1984). Periplasmic gel: new concept resulting from the reinvestigation of bacterial cell envelope ultrastructure by new methods. J. Bacteriol. 160, 143-152.
19. Huang, K. C., Ehrhardt, D. W., and Shaevitz, J. W. (2012). The molecular origins of chiral growth in walled cells. Curr. Opin. Microbiol. 15, 707-714. doi: 10.1016/j.mib.2012.11.002.
20. Huang, K. C., Mukhopadhyay, R., Wen, B., Gitai, Z., and Wingreen, N. S. (2008). Cell shape and cell-wall organization in Gram-negative bacteria. Proc. Natl. Acad. Sci. U.S.A. 105, 19282-19287. doi: 10.1073/pnas.0805309105.
21. Ishidate, K., Ursinus, A., Holtje, J. V., and Rothfield, L. (1998). Analysis of the length distribution of murein glycan strands in ftsZ and ftsI mutants of E. coli. FEMS Microbiol. Lett. 168, 71-75. doi: 10.1111/j.1574-6968.1998.tb13257.x.
22. Knaysi, G. (1930). The cell structure and cell division of Bacillus subtilis. J. Bacteriol. 19, 113-115.
23. Knaysi, G. (1941). Observations on the cell division of some yeasts and bacteria. J. Bacteriol. 41, 141-153.
24. Kuru, E., Hughes, H. V., Brown, P. J., Hall, E., Tekkam, S., Cava, F., et al. (2012). In Situ probing of newly synthesized peptidoglycan in live bacteria with fluorescent D-amino acids. Angew Chem. Int. Ed. Engl. 51, 12519-12523. doi: 10.1002/anie.201206749.
25. Labischinski, H., Goodell, E. W., Goodell, A., and Hochberg, M. L. (1991). Direct proof of a "more-than-single-layered" peptidoglycan architecture of Escherichia coli W7: a neutron small-angle scattering study. J. Bacteriol. 173, 751-756.
26. Lam, H., Oh, D. C., Cava, F., Takacs, C. N., Clardy, J., de Pedro, M. A., et al. (2009). D-amino acids govern stationary phase cell wall remodeling in bacteria. Science 325, 1552-1555. doi: 10.1126/science.1178123.
27. Lavollay, M., Arthur, M., Fourgeaud, M., Dubost, L., Marie, A., Veziris, N., et al. (2008). The peptidoglycan of stationary-phase Mycobacterium tuberculosis predominantly contains cross-links generated by L,D-transpeptidation. J. Bacteriol. 190, 4360-4366. doi: 10.1128/JB.00239-08.
28. Leps, B., Labischinski, H., and Bradaczek, H. (1987). Conformational behavior of the polysaccharide backbone of murein. Biopolymers 26, 1391-1406. doi: 10.1002/bip.360260813.
29. Magnet, S., Bellais, S., Dubost, L., Fourgeaud, M., Mainardi, J. L., Petit-Frere, S., et al. (2007). Identification of the L,D-transpeptidases responsible for attachment of the Braun lipoprotein to Escherichia coli peptidoglycan. J. Bacteriol. 189, 3927-3931. doi: 10.1128/JB.00084-07.
30. Magnet, S., Dubost, L., Marie, A., Arthur, M., and Gutmann, L. (2008). Identification of the L,D-transpeptidases for peptidoglycan cross-linking in Escherichia coli. J. Bacteriol. 190, 4782-4785. doi: 10.1128/JB.00025-08.
31. Meroueh, S. O., Bencze, K. Z., Hesek, D., Lee, M., Fisher, J. F., Stemmler, T. L., et al. (2006). Three-dimensional structure of the bacterial cell wall peptidoglycan. Proc. Natl. Acad. Sci. U.S.A. 103, 4404-4409. doi: 10.1073/pnas.0510182103.
32. Obermann, W., and Holtje, J. V. (1994). Alterations of murein structure and of penicillin-binding proteins in minicells from Escherichia coli. Microbiology 140(Pt 1), 79-87. doi: 10.1099/13500872-140-1-79.
33. Oldmixon, E. H., Glauser, S., and Higgins, M. L. (1974). Two proposed general configurations for bacterial cell wall peptidoglycans shown by space-filling molecular models. Biopolymers 13, 2037-2060. doi: 10.1002/bip.1974.360131008.
34. Pisabarro, A. G., de Pedro, M. A., and Vazquez, D. (1985). Structural modifications in the peptidoglycan of Escherichia coli associated with changes in the state of growth of the culture. J. Bacteriol. 161, 238-242.
35. Prats, R., and de Pedro, M. A. (1989). Normal growth and division of Escherichia coli with a reduced amount of murein. J. Bacteriol. 171, 3740-3745.
36. Primosigh, J., Pelzer, H., Maass, D., and Weidel, W. (1961). Chemical characterization of mucopeptides released from the E. coli B cell wall by enzymic action. Biochim. Biophys. Acta 46, 68-80. doi: 10.1016/0006-3002(61)90647-3.
37. Quintela, J. C., Caparros, M., and de Pedro, M. A. (1995). Variability of peptidoglycan structural parameters in gram-negative bacteria. FEMS Microbiol. Lett. 125, 95-100. doi: 10.1111/j.1574-6968.1995.tb07341.x.
38. Romeis, T., Kohlrausch, U., Burgdorf, K., and Holtje, J. V. (1991). Murein chemistry of cell division in Escherichia coli. Res. Microbiol. 142, 325-332. doi: 10.1016/0923-2508(91)90048-F.
39. Salton, M. R. (1952). Studies of the bacterial cell wall. III. Preliminary investigation of the chemical constitution of the cell wall of Streptococcus faecalis. Biochim. Biophys. Acta 8, 510-519. doi: 10.1016/0006-3002(52)90082-6.
40. Salton, M. R. (1953). Studies of the bacterial cell wall. IV. The composition of the cell walls of some Gram-positive and Gram-negative bacteria. Biochim. Biophys. Acta 10, 512-523. doi: 10.1016/0006-3002(53)90296-0.
41. Salton, M. R. (1956). Studies of the bacterial cell wall. V. The action of lysozyme on cell walls of some lysozyme-sensitive bacteria. Biochim. Biophys. Acta 22, 495-506. doi: 10.1016/0006-3002(56)90060-9.
42. Salton, M. R. (1960). Studies of the bacterial cell wall. VII. Monosaccharide constituents of the walls of gram-negative bacteria. Biochim. Biophys. Acta 45, 364-371. doi: 10.1016/0006-3002(60)91459-1.
43. Salton, M. R. (1961). Studies of the bacterial cell wall. VIII. Reaction of walls with hydrazine and with fluorodinitrobenzene. Biochim. Biophys. Acta 52, 329-342. doi: 10.1016/0006-3002(61)90682-5.
44. Salton, M. R., and Horne, R. W. (1951a). Studies of the bacterial cell wall. I. Electron microscopical observations on heated bacteria. Biochim. Biophys. Acta 7, 19-42. doi: 10.1016/0006-3002(51)90003-0.
45. Salton, M. R., and Horne, R. W. (1951b). Studies of the bacterial cell wall. II. Methods of preparation and some properties of cell walls. Biochim. Biophys. Acta 7, 177-197. doi: 10.1016/0006-3002(51)90017-0.
46. Schleifer, K. H., and Kandler, O. (1972). Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36, 407-477.
47. Siegrist, M. S., Whiteside, S., Jewett, J. C., Aditham, A., Cava, F., and Bertozzi, C. R. (2013). (D)-Amino acid chemical reporters reveal peptidoglycan dynamics of an intracellular pathogen. ACS Chem. Biol. 8, 500-505. doi: 10.1021/cb3004995.
48. Takacs, C. N., Poggio, S., Charbon, G., Pucheault, M., Vollmer, W., and Jacobs-Wagner, C. (2010). MreB drives de novo rod morphogenesis in Caulobacter crescentus via remodeling of the cell wall. J. Bacteriol. 192, 1671-1684. doi: 10.1128/JB.01311-09.
49. Typas, A., Banzhaf, M., Gross, C. A., and Vollmer, W. (2012). From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat. Rev. Microbiol. 10, 123-136. doi: 10.1038/nrmicro2677.
50. Ursinus, A., Van Den Ent, F., Brechtel, S., de Pedro, M., Holtje, J. V., Lowe, J., et al. (2004). Murein (peptidoglycan) binding property of the essential cell division protein FtsN from Escherichia coli. J. Bacteriol. 186, 6728-6737. doi: 10.1128/JB.186.20.6728-6737.2004.
51. van Heijenoort, J. (2001). Formation of the glycan chains in the synthesis of bacterial peptidoglycan. Glycobiology 11, 25R-36R. doi: 10.1093/glycob/11.3.25R.
52. Varma, A., de Pedro, M. A., and Young, K. D. (2007). FtsZ directs a second mode of peptidoglycan synthesis in Escherichia coli. J. Bacteriol. 189, 5692-5704. doi: 10.1128/JB.00455-07.
53. Vasstrand, E. N., Jensen, H. B., Miron, T., and Hofstad, T. (1982). Composition of peptidoglycans in Bacteroidaceae: determination and distribution of lanthionine. Infect. Immun. 36, 114-122.
54. Vollmer, W. (2008). Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol. Rev. 32, 287-306. doi: 10.1111/j.1574-6976.2007.00088.x.
55. Vollmer, W., Blanot, D., and de Pedro, M. A. (2008). Peptidoglycan structure and architecture. FEMS Microbiol. Rev. 32, 149-167. doi: 10.1111/j.1574-6976.2007.00094.x.
56. Weidel, W. (1960). Mucopolymers of the cell-wall of E. coli B. Bull. Soc. Chim. Biol. (Paris) 42, 1833-1835.
57. Weidel, W., Frank, H., and Martin, H. H. (1960). The rigid layer of the cell wall of Escherichia coli strain B. J. Gen. Microbiol. 22, 158-166. doi: 10.1099/00221287-22-1-158.
58. Weidel, W., and Pelzer, H. (1964). Bagshaped macromolecules-a new outlook on bacterial cell walls. Adv. Enzymol. Relat. Areas Mol. Biol. 26, 193-232.
59. Wientjes, F. B., Woldringh, C. L., and Nanninga, N. (1991). Amount of peptidoglycan in cell walls of gram-negative bacteria. J. Bacteriol. 173, 7684-7691.
60. Yao, X., Jericho, M., Pink, D., and Beveridge, T. (1999). Thickness and elasticity of gram-negative murein sacculi measured by atomic force microscopy. J. Bacteriol. 181, 6865-6875.